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Asymmetric interactions between doublesex and tissue- and sex-specific target genes mediate sexual dimorphism in beetles.

ABSTRACT: Sexual dimorphisms fuel significant intraspecific variation and evolutionary diversification. Yet the developmental-genetic mechanisms underlying sex-specific development remain poorly understood. Here, we focus on the conserved sex-determination gene doublesex (dsx) and the mechanisms by which it mediates sex-specific development in a horned beetle species by combining systemic dsx knockdown, high-throughput sequencing of diverse tissues and a genome-wide analysis of Dsx-binding sites. We find that Dsx regulates sex-biased expression predominantly in males, that Dsx's target repertoires are highly sex- and tissue-specific and that Dsx can exercise its regulatory role via two distinct mechanisms: as a sex-specific modulator by regulating strictly sex-specific targets, or as a switch by regulating the same genes in males and females in opposite directions. More generally, our results suggest Dsx can rapidly acquire new target gene repertoires to accommodate evolutionarily novel traits, evidenced by the large and unique repertoire identified in head horns, a recent morphological innovation.

SUBMITTER: Ledon-Rettig CC

PROVIDER: S-EPMC5333360 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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Asymmetric interactions between doublesex and tissue- and sex-specific target genes mediate sexual dimorphism in beetles.

Ledón-Rettig C C CC Zattara E E EE Moczek A P AP

Nature communications 20170227

Sexual dimorphisms fuel significant intraspecific variation and evolutionary diversification. Yet the developmental-genetic mechanisms underlying sex-specific development remain poorly understood. Here, we focus on the conserved sex-determination gene doublesex (dsx) and the mechanisms by which it mediates sex-specific development in a horned beetle species by combining systemic dsx knockdown, high-throughput sequencing of diverse tissues and a genome-wide analysis of Dsx-binding sites. We find ...[more]

PMID: 28239147

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Project description:Marrow adipose tissue (MAT) is unique with respect to origin, metabolism, and function. MAT is characterized with high heterogeneity which correlates with skeletal location and bone metabolism. This fat depot is also highly sensitive to various hormonal, environmental, and pharmacologic cues to which it responds with changes in volume and/or metabolic phenotype. We have demonstrated previously that MAT has characteristics of both white (WAT) and brown (BAT)-like or beige adipose tissue, and that beige phenotype is attenuated with aging and in diabetes. Here, we extended our analysis by comparing MAT phenotype in different locations within a tibia bone of mature C57BL/6 mice and with respect to the presence of sex steroids in males and females. We report that MAT juxtaposed to trabecular bone of proximal tibia (pMAT) is characterized by elevated expression of beige fat markers including Ucp1, HoxC9, Prdm16, Tbx1, and Dio2, when compared with MAT located in distal tibia (dMAT). There is also a difference in tissue organization with adipocytes in proximal tibia being dispersed between trabeculae, while adipocytes in distal tibia being densely packed. Higher trabecular bone mass (BV/TV) in males correlates with lower pMAT volume and higher expression of beige markers in the same location, when compared with females. However, there is no sexual divergence in the volume and transcriptional profile of dMAT. A removal of ovaries in females resulted in decreased cortical bone mass and increased volume of both pMAT and dMAT, as well as volume of gonadal WAT (gWAT). Increase in pMAT volume was associated with marked increase in Fabp4 and Adiponectin expression and relative decrease in beige fat gene markers. A removal of testes in males resulted in cortical and trabecular bone loss and the tendency to increased volume of both pMAT and dMAT, despite a loss of gWAT. Orchiectomy did not affect the expression of white and beige adipocyte gene markers. In conclusion, expression profile of beige adipocyte gene markers correlates with skeletal location of active bone remodeling and higher BV/TV, however bone loss resulted from sex steroid deficiency is not proportional to MAT expansion at the same skeletal location.

Dataset Information

Asymmetric interactions between doublesex and tissue- and sex-specific target genes mediate sexual dimorphism in beetles.

Publications

Asymmetric interactions between doublesex and tissue- and sex-specific target genes mediate sexual dimorphism in beetles.

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